Hair plate

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Hair plates are a type of proprioceptor found in the folds of insect joints[1]. They consist of a cluster of hairs, in which each hair is innervated by a single mechanosensory neuron. Functionally, hair plates operate as "limit-detectors" by signaling the extremes of joint movement [2], which then drives reflexive leg movement[3].

Hair plate location and anatomy[edit]

Figure.1 Schematic of a hair plate. Hair plates are positioned next to folds within the cuticle, so that the deflection of the hairs signal the relative movements of adjoining body or leg segments.

Hair plates consist of a field of cuticular hairs, in which each hair is innervated by a single mechanosensory neuron[1] [4](Figure 1). Hair plates are positioned within folds of cuticle at joints, and the associated hairs are deflected during joint movement[5]. The number of hairs across and within hair plates can vary[6][7] and hair plates are found on different body parts, including the legs,[8][9][10][6][11] neck,[12][13] and antennae.[14][15] On the legs of insects, hair plates are found at the proximal joints (i.e. thorax-coxa, coxa-trochanter, and trochanter-femur joints) across the front, middle, and hind legs.

Hair plate neurons project into the ventral nerve cord where the arborize dorsally and around the leg neuromere [16]. Moreover, the neurons of the hair plates located at the thorax-coxa joint project through the ventral, dorsal, and accessory prothoracic nerves, whereas, other hair plate neurons on the leg project through the prothoracic leg nerve[17][18]. Lastly, the neurons from each hair plate may have distinct axonal morphologies.

Sensory encoding and feedback circuits[edit]

Hair-plates are proprioceptors[1] and provide information to the nervous system about the positional and movement state of the body and legs. Hair plate neurons come in two flavors, one that responds phasically (rapidly adapting) and another that responds tonically (slowly adapting) to transient or maintained deflections of the hairs[11][19]. These encoding properties enable hair plates to signal the position and movement of adjoining body or leg segments. Neurons associated with the longer hairs within a hair plate form direct, mono-synaptic excitatory chemical synapses with motor neurons[6] as well as synapses with non-spiking interneurons that provide inhibitory input onto antagonistic motor neurons[20]. Therefore, hair plates provide rapid feedback to control the movement direction of the leg they are located on. It remains unknown what information the smaller hairs of hair plates signal and what that information is used for in leg motor control. Hair plate neurons are also involved in the presynaptic inhibition to other proprioceptors.[21]

Hair plate feedback to control behavior[edit]

Walking[edit]

Hair plates located at the leg joints provide sensory feedback for the control of walking[8][9][22][2][23][24][25]. In stick insects and cockroaches, the surgical removal of coxa hair plates alter the extremes of leg movement in such a way that the leg may overstep and collide with an ipsilateral leg. Therefore, hair plates control the transition of leg movement direction as well as the extent to which legs travel during the step cycle [8][22]. This “limit-detector” function is similar to that of mammalian joint receptors[26]. Therefore, hair plates encode the extremes of joint movement during walking to precisely control the direction of leg movement.

Feeding[edit]

Mechanosensory information from front leg hair plates also contribute to the regulation of feeding behavior in fruit flies, Drosophila melanogaster[27]. Integration of hair plate mechanosensory information with olfactory information from antennal neurons control the proboscis extension reflex (PER) in flies. Thus, the sensory input from hair plates is integrated with the information from other sensory modalities to control behaviors beyond walking.

Posture[edit]

Hair plates located on the neck (known as the prosternal organ) monitor head position relative to the thorax and provide sensory feedback for the control of head posture.[12][13] In the blowfly Calliphora, surgical removal of the prosternal organ hairs on one side causes the fly to compensate by rolling the head toward the operated side.[12] These results suggest that the prosternal organ may be involved in gaze stabilization.

Hair plates on the legs have also been shown to be important for resting posture. The ablation of the anterior trochanteral hair plate on a stick insect leg did not alter the coordination between legs, but rather resulted in that leg being held higher[28]. Also, hair plates on the trochanter were shown to control the body height. Overall, in addition to controlling walking kinematics, hair plates are also involved in postural control.

Antennal movement[edit]

Hair plates located on the proximal segments of the antenna (Figure 2) provide sensory feedback for the control of antennal movement[15] and are thought to play an important role in active sensing, object localization, and targeted reaching movements[14][29].

Figure. 2 Lateral view of a cockroach antenna, showing the hair plates at the base.

See also[edit]

References[edit]

  1. ^ a b c Tuthill; Wilson (2016). "Mechanosensation and Adaptive Motor Control in Insects". Current Biology. 26 (20): R1022–R1038. doi:10.1016/j.cub.2016.06.070. PMC 5120761. PMID 27780045.
  2. ^ a b Bässler, U. (1977-06-01). "Sensory control of leg movement in the stick insect Carausius morosus". Biological Cybernetics. 25 (2): 61–72. doi:10.1007/BF00337264. ISSN 1432-0770. PMID 836915. S2CID 2634261.
  3. ^ Burrows, Malcolm (1996-09-26). The Neurobiology of an Insect Brain. Oxford University Press. ISBN 978-0-19-172441-1.
  4. ^ Pringle, J (1938). "Proprioception in Insects: III. The Function of the Hair Sensilla at the Joints". JEB. 15 (4): 467–473.
  5. ^ Pringle, J. W. S. (1938-10-01). "Proprioception In Insects: III. The Function Of The Hair Sensilla At The Joints". Journal of Experimental Biology. 15 (4): 467–473. doi:10.1242/jeb.15.4.467. ISSN 0022-0949.
  6. ^ a b c Pearson; Wong; Fourtner (1976). "Connexions between hair-plate afferents and motorneurones in the cockroach leg". J Exp Biol. 64 (1): 251–266. doi:10.1242/jeb.64.1.251. PMID 5571.
  7. ^ Petryszak, Anna (1994). "External proprioceptors on the legs of insects of higher orders". Acta Biologica Cracoveinsia. 36: 13–22.
  8. ^ a b c Wendler, Gernot (1964-03-01). "Laufen und Stehen der Stabheuschrecke Carausius morosus: Sinnesborstenfelder in den Beingelenken als Glieder von Regelkreisen". Zeitschrift für vergleichende Physiologie (in German). 48 (2): 198–250. doi:10.1007/BF00297860. ISSN 1432-1351. S2CID 37588295.
  9. ^ a b Markl, Hubert (1962-09-01). "Borstenfelder an den Gelenken als Schweresinnesorgane bei Ameisen und anderen Hymenopteren". Zeitschrift für vergleichende Physiologie (in German). 45 (5): 475–569. doi:10.1007/BF00342998. ISSN 1432-1351. S2CID 38336445.
  10. ^ Murphey, R. K.; Possidente, Debra; Pollack, Gerald; Merritt, D. J. (1989). "Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila". Journal of Comparative Neurology. 290 (2): 185–200. doi:10.1002/cne.902900203. ISSN 1096-9861. PMID 2512333. S2CID 6726012.
  11. ^ a b Newland; Watkins; Emptage; Nagayama (1976). "The structure, response properties, and development of a hair plate on the mesothoracic leg of the locust". J Exp Biol. 64: 233–249.
  12. ^ a b c Preuss; Hengstenberg (1992). "Structure and kinematics of the prosternal organs and their influence on head position in the blowfly Calliphora erythocephala". J Comp Physiol. 171: 483–493. doi:10.1007/BF00194581. S2CID 13379331.
  13. ^ a b Paulk; Gilbert (2006). "Proprioceptive encoding of head position in the black soldier fly, Hermetia illucens". J Exp Biol. 209 (Pt 19): 3913–3924. doi:10.1242/jeb.02438. PMID 16985207. S2CID 12169844.
  14. ^ a b Okada; Toh (2000). "The role of antennal hair plates in object-guided tactile orientation of the cockroach". Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology. 186 (9): 849–857. doi:10.1007/s003590000137. PMID 11085638. S2CID 1917793.
  15. ^ a b Krause, André F.; Winkler, Andrea; Dürr, Volker (January 2013). "Central drive and proprioceptive control of antennal movements in the walking stick insect". Journal of Physiology, Paris. 107 (1–2): 116–129. doi:10.1016/j.jphysparis.2012.06.001. ISSN 1769-7115. PMID 22728470. S2CID 11851224.
  16. ^ Merritt, D. J.; Murphey, R. K. (1992-08-01). "Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion". The Journal of Comparative Neurology. 322 (1): 16–34. doi:10.1002/cne.903220103. ISSN 0021-9967. PMID 1430308. S2CID 10317647.
  17. ^ Kuan, Aaron T.; Phelps, Jasper S.; Thomas, Logan A.; Nguyen, Tri M.; Han, Julie; Chen, Chiao-Lin; Azevedo, Anthony W.; Tuthill, John C.; Funke, Jan; Cloetens, Peter; Pacureanu, Alexandra (December 2020). "Dense neuronal reconstruction through X-ray holographic nano-tomography". Nature Neuroscience. 23 (12): 1637–1643. doi:10.1038/s41593-020-0704-9. ISSN 1546-1726. PMC 8354006. PMID 32929244.
  18. ^ Phelps, Jasper S.; Hildebrand, David Grant Colburn; Graham, Brett J.; Kuan, Aaron T.; Thomas, Logan A.; Nguyen, Tri M.; Buhmann, Julia; Azevedo, Anthony W.; Sustar, Anne; Agrawal, Sweta; Liu, Mingguan (2021-02-04). "Reconstruction of motor control circuits in adult Drosophila using automated transmission electron microscopy". Cell. 184 (3): 759–774.e18. doi:10.1016/j.cell.2020.12.013. ISSN 0092-8674. PMC 8312698. PMID 33400916.
  19. ^ French; Wong (1976). "The responses of trochanteral hair plate sensilla in the cockroach to periodic and random displacements". Biol. Cyber. 22: 33–38. doi:10.1007/BF00340230. S2CID 9672599.
  20. ^ Büschges, Ansgar; Schmitz, Josef (April 1991). "Nonspiking pathways antagonize the resistance reflex in the thoraco‐coxal joint of stick insects". Journal of Neurobiology. 22 (3): 224–237. doi:10.1002/neu.480220303. ISSN 0022-3034.
  21. ^ Stein; Schmitz (1999). "Multimodal convergence of presynaptic afferent inhibition in insect proprioceptors". Neurophysiology. 82 (1): 512–514. doi:10.1152/jn.1999.82.1.512. PMID 10400981.
  22. ^ a b Wong; Pearson (1976). "Properties of the trochanteral hair plate and its function in the control of walking in the cockroach". J Exp Biol. 64 (1): 233–249. doi:10.1242/jeb.64.1.233. PMID 1270992.
  23. ^ Cruse, H.; Dean, J.; Suilmann, M. (1984-09-01). "The contributions of diverse sense organs to the control of leg movement by a walking insect". Journal of Comparative Physiology A. 154 (5): 695–705. doi:10.1007/BF01350223. ISSN 1432-1351. S2CID 2519441.
  24. ^ Schmitz, J. (1986-10-01). "The depressor trochanteris motoneurones and their role in the coxo-trochanteral feedback loop in the stick insect Carausius morosus". Biological Cybernetics. 55 (1): 25–34. doi:10.1007/BF00363975. ISSN 1432-0770. S2CID 23692174.
  25. ^ Theunissen, Leslie M.; Vikram, Subhashree; Dürr, Volker (2014-09-15). "Spatial co-ordination of foot contacts in unrestrained climbing insects". Journal of Experimental Biology. 217 (18): 3242–3253. doi:10.1242/jeb.108167. ISSN 0022-0949. PMID 25013102.
  26. ^ Tuthill, John C.; Azim, Eiman (5 March 2018). "Proprioception". Current Biology. 28 (5): R194–R203. doi:10.1016/j.cub.2018.01.064. ISSN 1879-0445. PMID 29510103.
  27. ^ Oh, Soo Min; Jeong, Kyunghwa; Seo, Jeong Taeg; Moon, Seok Jun (2021-02-16). "Multisensory interactions regulate feeding behavior in Drosophila". Proceedings of the National Academy of Sciences. 118 (7): e2004523118. Bibcode:2021PNAS..11804523O. doi:10.1073/pnas.2004523118. ISSN 0027-8424. PMC 7896327. PMID 33558226.
  28. ^ Burrows, Malcolm (1996). The Neurobiology of an Insect Brain. Oxford. ISBN 9780198523444.
  29. ^ Schütz, Christoph; Dürr, Volker (2011-11-12). "Active tactile exploration for adaptive locomotion in the stick insect". Philosophical Transactions of the Royal Society B: Biological Sciences. 366 (1581): 2996–3005. doi:10.1098/rstb.2011.0126. ISSN 0962-8436. PMC 3172591. PMID 21969681.
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